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Selection on Phalanx Development in the Evolution of the Bird Wing

The frameshift hypothesis is a widely accepted model of bird wing evolution. This hypothesis postulates a shift in positional values, or molecular-developmental identity, that caused a change in digit phenotype. The hypothesis synthesized developmental and paleontological data on wing digit homology...

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Autores principales: de Bakker, Merijn A G, van der Vos, Wessel, de Jager, Kaylah, Chung, Wing Yu, Fowler, Donald A, Dondorp, Esther, Spiekman, Stephan N F, Chew, Keng Yih, Xie, Bing, Jiménez, Rafael, Bickelmann, Constanze, Kuratani, Shigeru, Blazek, Radim, Kondrashov, Peter, Renfree, Marilyn B, Richardson, Michael K
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8476175/
https://www.ncbi.nlm.nih.gov/pubmed/34164688
http://dx.doi.org/10.1093/molbev/msab150
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author de Bakker, Merijn A G
van der Vos, Wessel
de Jager, Kaylah
Chung, Wing Yu
Fowler, Donald A
Dondorp, Esther
Spiekman, Stephan N F
Chew, Keng Yih
Xie, Bing
Jiménez, Rafael
Bickelmann, Constanze
Kuratani, Shigeru
Blazek, Radim
Kondrashov, Peter
Renfree, Marilyn B
Richardson, Michael K
author_facet de Bakker, Merijn A G
van der Vos, Wessel
de Jager, Kaylah
Chung, Wing Yu
Fowler, Donald A
Dondorp, Esther
Spiekman, Stephan N F
Chew, Keng Yih
Xie, Bing
Jiménez, Rafael
Bickelmann, Constanze
Kuratani, Shigeru
Blazek, Radim
Kondrashov, Peter
Renfree, Marilyn B
Richardson, Michael K
author_sort de Bakker, Merijn A G
collection PubMed
description The frameshift hypothesis is a widely accepted model of bird wing evolution. This hypothesis postulates a shift in positional values, or molecular-developmental identity, that caused a change in digit phenotype. The hypothesis synthesized developmental and paleontological data on wing digit homology. The “most anterior digit” (MAD) hypothesis presents an alternative view based on changes in transcriptional regulation in the limb. The molecular evidence for both hypotheses is that the MAD expresses Hoxd13 but not Hoxd11 and Hoxd12. This digit I “signature” is thought to characterize all amniotes. Here, we studied Hoxd expression patterns in a phylogenetic sample of 18 amniotes. Instead of a conserved molecular signature in digit I, we find wide variation of Hoxd11, Hoxd12, and Hoxd13 expression in digit I. Patterns of apoptosis, and Sox9 expression, a marker of the phalanx-forming region, suggest that phalanges were lost from wing digit IV because of early arrest of the phalanx-forming region followed by cell death. Finally, we show that multiple amniote lineages lost phalanges with no frameshift. Our findings suggest that the bird wing evolved by targeted loss of phalanges under selection. Consistent with our view, some recent phylogenies based on dinosaur fossils eliminate the need to postulate a frameshift in the first place. We suggest that the phenotype of the Archaeopteryx lithographica wing is also consistent with phalanx loss. More broadly, our results support a gradualist model of evolution based on tinkering with developmental gene expression.
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spelling pubmed-84761752021-09-28 Selection on Phalanx Development in the Evolution of the Bird Wing de Bakker, Merijn A G van der Vos, Wessel de Jager, Kaylah Chung, Wing Yu Fowler, Donald A Dondorp, Esther Spiekman, Stephan N F Chew, Keng Yih Xie, Bing Jiménez, Rafael Bickelmann, Constanze Kuratani, Shigeru Blazek, Radim Kondrashov, Peter Renfree, Marilyn B Richardson, Michael K Mol Biol Evol Discoveries The frameshift hypothesis is a widely accepted model of bird wing evolution. This hypothesis postulates a shift in positional values, or molecular-developmental identity, that caused a change in digit phenotype. The hypothesis synthesized developmental and paleontological data on wing digit homology. The “most anterior digit” (MAD) hypothesis presents an alternative view based on changes in transcriptional regulation in the limb. The molecular evidence for both hypotheses is that the MAD expresses Hoxd13 but not Hoxd11 and Hoxd12. This digit I “signature” is thought to characterize all amniotes. Here, we studied Hoxd expression patterns in a phylogenetic sample of 18 amniotes. Instead of a conserved molecular signature in digit I, we find wide variation of Hoxd11, Hoxd12, and Hoxd13 expression in digit I. Patterns of apoptosis, and Sox9 expression, a marker of the phalanx-forming region, suggest that phalanges were lost from wing digit IV because of early arrest of the phalanx-forming region followed by cell death. Finally, we show that multiple amniote lineages lost phalanges with no frameshift. Our findings suggest that the bird wing evolved by targeted loss of phalanges under selection. Consistent with our view, some recent phylogenies based on dinosaur fossils eliminate the need to postulate a frameshift in the first place. We suggest that the phenotype of the Archaeopteryx lithographica wing is also consistent with phalanx loss. More broadly, our results support a gradualist model of evolution based on tinkering with developmental gene expression. Oxford University Press 2021-06-23 /pmc/articles/PMC8476175/ /pubmed/34164688 http://dx.doi.org/10.1093/molbev/msab150 Text en © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Discoveries
de Bakker, Merijn A G
van der Vos, Wessel
de Jager, Kaylah
Chung, Wing Yu
Fowler, Donald A
Dondorp, Esther
Spiekman, Stephan N F
Chew, Keng Yih
Xie, Bing
Jiménez, Rafael
Bickelmann, Constanze
Kuratani, Shigeru
Blazek, Radim
Kondrashov, Peter
Renfree, Marilyn B
Richardson, Michael K
Selection on Phalanx Development in the Evolution of the Bird Wing
title Selection on Phalanx Development in the Evolution of the Bird Wing
title_full Selection on Phalanx Development in the Evolution of the Bird Wing
title_fullStr Selection on Phalanx Development in the Evolution of the Bird Wing
title_full_unstemmed Selection on Phalanx Development in the Evolution of the Bird Wing
title_short Selection on Phalanx Development in the Evolution of the Bird Wing
title_sort selection on phalanx development in the evolution of the bird wing
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8476175/
https://www.ncbi.nlm.nih.gov/pubmed/34164688
http://dx.doi.org/10.1093/molbev/msab150
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